Due to small body size, an immature musculoskeletal system, and other growth‐related limits on performance, juvenile mammals frequently experience a greater risk of predation than their adult counterparts. As a result, behaviorally precocious juveniles are hypothesized to exhibit musculoskeletal advantages that permit them to accelerate rapidly and evade predation. This hypothesis was tested through detailed quantitative evaluation of muscle growth in wild Eastern cottontail rabbits (
For many animals, the juvenile stage of life can be particularly perilous. Once independent, immature animals must often complete the same basic survival functions as adults despite smaller body size and other growth-related limits on performance. Because, by definition, juveniles have yet to reproduce, we should expect strong selection for mechanisms to offset these ontogenetic limitations, allowing individuals to reach reproductive adulthood and maintain Darwinian fitness. We use an integrated ontogenetic dataset on morphology, locomotor performance, and longevity in wild cottontail rabbits (Sylvilagus floridanus, Allen 1848) to test the hypothesis that prey animals are under selective pressure to maximize juvenile performance. We predicted that (1) juveniles would accelerate more quickly than adults, allowing them to reach adult-like escape speeds, and (2) juveniles with greater levels of performance should survive for longer durations in the wild, thus increasing their reproductive potential. Using high-speed video and force platform measurements, we quantified burst acceleration, escape speed, and mechanical power production in 38 wild-caught S. floridanus (26 juveniles, 12 adults; all rabbits >1 kg in body mass were designated to be adults, based on published growth curves and evidence of epiphyseal fusion). A subsample of 22 rabbits (15 juveniles, 7 adults) was fitted with radio-telemetry collars for documenting survivorship in the wild. We found that acceleration and escape speed peaked in the late juvenile period in S. floridanus, at an age range that coincides with a period of pronounced demographic attrition in wild populations. Differences in mass-specific mechanical power production explained ∼75% of the variation in acceleration across the dataset, indicating that juvenile rabbits outpace adults by producing more power per unit body mass. We found a positive, though non-significant, association between peak escape speed and survivorship duration in the wild, suggesting a complex relationship between locomotor performance and fitness in growing S. floridanus.
more » « less- NSF-PAR ID:
- 10362401
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative Organismal Biology
- Volume:
- 4
- Issue:
- 1
- ISSN:
- 2517-4843
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Sylvilagus floridanus ). Cottontail rabbits experience high rates of mortality during the first year of life, suggesting that selection might act to improve performance in growing juveniles. Therefore, it was predicted that muscle properties associated with force and power capacity should be enhanced in juvenile rabbits to facilitate enhanced locomotor performance. We quantified muscle architecture from 24 paravertebral and hindlimb muscles across ontogeny in a sample of n =MM ), physiological cross‐sectional area (PCSA ), isometric force (F max), and instantaneous power (P inst), along with several dimensionless architectural indices. In contrast to our hypothesis,MM andPCSA for most muscles change with positive allometry during growth by scaling atand , respectively, whereas F maxandP instgenerally scale indistinguishably from isometry, as do the architectural indices tested. However, scaling patterns indicate that the digital flexors and ankle extensors of juvenileS. floridanus have greater capacities for force and power, respectively, than those in adults, suggesting these muscle properties may be a part of several compensatory features that promote enhanced acceleration performance in young rabbits. Overall, our study implies that body size constraints place larger, more mature rabbits at a disadvantage during acceleration, and that adults must develop hypertrophied muscles in order to maintain mechanical similarity in force and power capacities across development. These findings challenge the accepted understanding that juvenile animals are at a performance detriment relative to adults. Instead, for prey–predator interactions necessitating short intervals of high force and power generation relative to body mass, as demonstrated by rapid acceleration of cottontail rabbits fleeing predators, it may be the adults that struggle to keep pace with juveniles. -
Kaiser, Hinrich ; Zagar, Anamarija ; Müller, Hendrik (Ed.)Abstract. Marking juveniles of terrestrial direct-developing frogs is challenging because of their small size (< 18 mm) and fragility. This difficulty has limited studies on demography or population dynamics where empirical data on the survivorship of juveniles or their recruitment to adulthood are missing. In a controlled laboratory experiment, we tested the survivorship of wild-caught juvenile Eleutherodactylus coqui Thomas, 1966 to marking with a single colour visual internal elastomer (VIE) in the thigh, with and without additional ventral skin-swabbing for disease or microbiome monitoring. Results revealed 100% survival in all groups, and all juveniles remained unharmed, moved freely, and fed actively during three days after treatment, suggesting that this type of manipulation does not cause direct mortality. After 17 months of the experiment, we have recaptured 11% of the marked juveniles as adults, indicating that they can survive to recruitment age. We propose the use of a single VIE colour as a method to mark and follow date-specific cohorts of juvenile direct-developing frogs or young metamorphs until they reach older and larger age classes. This marking method can be used safely together with skin swabbing and provide valuable information for studies on population biology and age-specific response to environmental or disease stressors.more » « less
-
Birds are well known for their ability to fly, and flight-capable adult birds have many anatomical specializations for meeting the demands of aerial locomotion. Juvenile birds in altricial species typically acquire these specializations close to fledging and leave the nest with some flight capability. In contrast, juveniles in most precocial species begin navigating their environment with rudimentary anatomies and may not develop full-sized wings or musculoskeletal apparatuses for several months. This manuscript explores how juvenile birds achieve high levels of locomotor performance in the absence of flight specializations, by synthesizing work on two groups of precocial birds with very different developmental strategies. Galliforms like the Chukar Partridge (Alectoris chukar) have early wing development and are capable of flight within weeks. Compared with adults, juvenile chukars have less aerodynamically effective feathers and smaller muscles but compensate through anatomical, kinematic, and behavioral mechanisms. In contrast, waterfowl have delayed wing development and initially rely on leg-based locomotion. In Mallards (Anas platyrhynchos) and their domesticated derivatives, leg investment and performance peak early in ontogeny, but then decline when wings develop. Chukar and mallard juveniles thus rely on different mechanisms for negotiating their surroundings in the absence of flight specializations. In conjunction with work in other animals, these patterns indicate that juveniles with developing locomotor apparatuses can achieve surprisingly high levels of locomotor performance through a variety of compensatory mechanisms.more » « less
-
more » « less
Synopsis Birds are well known for their ability to fly, and flight-capable adult birds have many anatomical specializations for meeting the demands of aerial locomotion. Juvenile birds in altricial species typically acquire these specializations close to fledging and leave the nest with some flight capability. In contrast, juveniles in most precocial species begin navigating their environment with rudimentary anatomies and may not develop full-sized wings or musculoskeletal apparatuses for several months. This manuscript explores how juvenile birds achieve high levels of locomotor performance in the absence of flight specializations, by synthesizing work on two groups of precocial birds with very different developmental strategies. Galliforms like the Chukar Partridge (Alectoris chukar) have early wing development and are capable of flight within weeks. Compared with adults, juvenile chukars have less aerodynamically effective feathers and smaller muscles but compensate through anatomical, kinematic, and behavioral mechanisms. In contrast, waterfowl have delayed wing development and initially rely on leg-based locomotion. In Mallards (Anas platyrhynchos) and their domesticated derivatives, leg investment and performance peak early in ontogeny, but then decline when wings develop. Chukar and mallard juveniles thus rely on different mechanisms for negotiating their surroundings in the absence of flight specializations. In conjunction with work in other animals, these patterns indicate that juveniles with developing locomotor apparatuses can achieve surprisingly high levels of locomotor performance through a variety of compensatory mechanisms.
-
more » « less
Abstract Assessing the factors that contribute to successful locomotor performance can provide critical insight into how animals survive in challenging habitats. Locomotion is powered by muscles, so that differences in the relative proportions of red (slow‐oxidative) vs. white (fast‐glycolytic) fibers can have significant implications for locomotor performance. We compared the relative proportions of axial red muscle fibers between groups of juveniles of the amphidromous gobiid fish,
Sicyopterus stimpsoni , from the Hawaiian Islands. Juveniles of this species migrate from the ocean into freshwater streams, navigating through a gauntlet of predators that require rapid escape responses, before reaching waterfalls which must be climbed (using a slow, inching behavior) to reach adult breeding habitats. We found that fish from Kaua'i have a smaller proportion of red fibers in their tail muscles than fish from Hawai'i, matching expectations based on the longer pre‐waterfall stream reaches of Kaua'i that could increase exposure to predators, making reduction of red muscle and increases in white muscle advantageous. However, no difference in red muscle proportions was identified between fish that were either successful or unsuccessful in scaling model waterfalls during laboratory climbing trials, suggesting that proportions of red muscle are near a localized fitness peak among Hawaiian individuals.
